Neural substrate of the late positive potential in emotional processing

Abstract

The late positive potential (LPP) is a reliable electrophysiological index of emotional perception in humans. Despite years of research, the brain structures that contribute to the generation and modulation of LPP are not well understood. Recording EEG and fMRI simultaneously, and applying a recently proposed single-trial ERP analysis method, we addressed the problem by correlating the single-trial LPP amplitude evoked by affective pictures with the blood oxygen level-dependent (BOLD) activity. Three results were found. First, relative to neutral pictures, pleasant and unpleasant pictures elicited enhanced LPP, as well as heightened BOLD activity in both visual cortices and emotion-processing structures such as amygdala and prefrontal cortex, consistent with previous findings. Second, the LPP amplitude across three picture categories was significantly correlated with BOLD activity in visual cortices, temporal cortices, amygdala, orbitofrontal cortex, and insula. Third, within each picture category, LPP-BOLD coupling revealed category-specific differences. For pleasant pictures, the LPP amplitude was coupled with BOLD in occipitotemporal junction, medial prefrontal cortex, amygdala, and precuneus, whereas for unpleasant pictures significant LPP-BOLD correlation was observed in ventrolateral prefrontal cortex, insula, and posterior cingulate cortex. These results suggest that LPP is generated and modulated by an extensive brain network composed of both cortical and subcortical structures associated with visual and emotional processing and the degree of contribution by each of these structures to the LPP modulation is valence specific.

Figure 1.

ERP analysis. A, Grand average (n = 11 subjects) ERP showing the LPP at Pz with time 0 set to the onset of pictures. B, The scalp topography showing the ERP difference between pleasant and neutral conditions. Here, ERP was averaged within the time interval from 300 to 600 ms. C, The scalp topography showing the ERP difference between unpleasant and neutral conditions. Here, ERP was averaged within the same interval.

Figure 2.

Single-trial ERP analysis. A, Epoched EEG data at Pz from a representative subject after artifact removal. B, Single-trial ERPs estimated using ASEO from data shown in A. C, Raster plot of the EEG data in A (smoothed with a moving average across 5 trials for visualization purpose). D, Raster plot of single-trial ERP data in B smoothed the same way as in C. E, Comparison between AERP using data in A and averaged ASEO single-trial ERPs (ASEO AERP) using data in B.

Figure 3.

Single-trial LPP dynamics. A, Trial-by-trial LPP amplitude for the pleasant and neutral conditions. B, Trial-by-trial LPP amplitude for the unpleasant and neutral conditions. The horizontal axes in A and B represent the sequential index of picture presentation within each picture category. C, Schematic illustrating the use of single-trial LPP amplitude as a parametric modulation in GLM. The height of each boxcar function is scaled by the mean-removed LPP amplitude.

Figure 4.

Activation maps based on BOLD contrast. A, Pleasant versus neutral (P vs N) condition. B, Unpleasant versus neutral (U vs N) condition. Activations are thresholded at p = 0.05 FDR corrected. PPC, Posterior parietal cortex; OFC, orbital frontal cortex; MPFC, medial prefrontal cortex; OTJ, occipitotemporal junction; AMYG, amygdala; HIPP, hippocampus; TP, temporal pole; SMA, supplementary motor area; VLPFC, ventral lateral prefrontal cortex; INS, insula.

Figure 5.

LPP–BOLD coupling maps in which highlighted regions indicate significant correlation between trial-by-trial fMRI response and the corresponding single-trial LPP amplitude. A, Pleasant, neutral, and unpleasant combined. B, Pleasant. C, Unpleasant. All maps are thresholded at p = 0.003. A cluster threshold k = 5 is further applied. OTJ, Occipitotemporal junction; INS, insula; AMYG, amygdala; HIPP, hippocampus; TP, temporal pole; PCu, precuneus; PCC, posterior cingulate cortex; MPFC, medial prefrontal cortex; VLPFC, ventrolateral prefrontal cortex; NAcc, nucleus accumbens.